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Abstract

Background

Few studies have examined whether dietary factors might affect blood pressure in children.
We purposed to investigate whether seaweed intake is associated with blood pressure
level among Japanese preschool children.

Methods

The design of the study was cross-sectional and it was conducted in autumn 2006. Subjects
were healthy preschoolers aged 3-6 years in Aichi, Japan. Blood pressure and pulse
were measured once by an automated sphygmomanometer, which uses oscillometric methods.
Dietary data, including seaweed intake, were assessed using 3-day dietary records
covering 2 consecutive weekdays and 1 weekend day. Of a total of 533 children, 459
(86.1 percent) agreed to be enrolled in our study. Finally, blood pressure measurement,
complete dietary records and parent-reported height and weight were obtained for 223
boys and 194 girls.

Conclusion

Our study showed that seaweed intake was negatively related to diastolic blood pressure
in boys and to systolic blood pressure in girls. This suggests that seaweed might
have beneficial effects on blood pressure among children.

Keywords:

blood pressure; child, preschool; diet records; seaweed; nutrition

Background

Hypertension, which often coexists with diabetes, dyslipidemia and obesity, promotes
atherosclerosis and contributes to the development of cardiovascular disease [1]. Hypertension is generally unusual among children, but many studies have shown the
tracking of blood pressure from childhood to adulthood [2], and some studies have indicated that the process of atherosclerosis starts in childhood
[3,4]. Thus, early intervention for high blood pressure is important in order to prevent
cardiovascular disease later in life.

Although there is much evidence for dietary risk factors for hypertension in adults
[5-13], few studies of children have been reported [14-21]. Restricted salt intake and reduced alcohol consumption are recommended for adults
[6]. The Dietary Approaches to Stop Hypertension (DASH diet), which is rich in fruits,
vegetables and low-fat dairy products, has beneficial effects on blood pressure among
adults [5-8]. The diet is rich in potassium and calcium, which have been reported to reduce blood
pressure among adults [8,9,13]. A negative association between magnesium and blood pressure has also been reported
among adults in some papers [10,11,13]. However, the role of diet in blood pressure among children is not well understood.

Seaweeds are traditional Japanese foods, and are consumed as they are (nori, kombu,
hijiki) or as ingredients of rice balls (nori) and salads or soups (wakame). Seaweeds
contain large quantities of dietary fiber, minerals, vitamins and polysaccharides
[22]. Several experimental studies in animals [23-27] have shown that feeding on seaweed or its extract lowers blood pressure, suggesting
that seaweed intake might affect blood pressure in humans. However, only a few epidemiological
studies have reported an association between seaweed intake and blood pressure, and
the results have been inconsistent [28-31]. These studies were conducted among adults, and the relationship of seaweed intake
to blood pressure has not been investigated among children.

In this study, we purposed to investigate whether dietary seaweed intake is associated
with blood pressure level among Japanese preschool children. We hypothesized that
seaweed might beneficially affect blood pressure among children.

Methods

Subjects and Design

Subjects were children aged three to six years who attended one of two preschools
in Aichi Prefecture, Japan. The details of the cohorts have been described elsewhere
previously [32]. During October and November 2006, they underwent blood pressure measurement. Urine,
which was first voided after a child waked up, was collected. Children's height, weight,
health status, and lifestyles were inquired through a parent-administered questionnaire.
Lifestyles included the time when they got up or went to bed, and a nap time. Physical
activity was based on an outdoor playtime checklist by Burdette et al. [33]. The parents were also asked to record the children's dietary intake for covering
2 consecutive weekdays and 1 weekend day. Of a total of 533 preschool children, 459
(86.1 percent) agreed to be enrolled in our study, with their parents providing written
informed consent. Finally, blood pressure measurement, complete dietary records and
parent-reported height and weight were obtained for 417 of the children. This study
protocol and the informed consent procedure were approved by the ethical board of
Gifu University Graduate School of Medicine, Gifu, Japan.

Dietary data

To collect nutritional data, diet including seaweed intake was assessed using 3-day
dietary records covering 2 consecutive weekdays and 1 weekend day. The parents received
written instructions on recording the food intakes of the children. According to the
instructions, they recorded the amount and kind of foods, beverages and dishes which
were consumed by their children during each of three days. When they were in trouble
with recording, our stuffs assisted them on the phone. Because our subjects usually
ate a school-provided lunch, we obtained the menus from each kindergarten and our
staffs, which were dieticians, checked the quantity left over after each meal. Individual
nutrient intake was estimated using the Japanese Standard Table of Food Composition,
5th revised and enlarged edition [22]. We calculated energy intake in kilocalories per day and seaweed and salt intake
in grams per day. Seaweed intake was converted to dry volume units.

Blood pressure and other measurements

Systolic (SBP), diastolic blood pressure (DBP) and pulse were measured once by an
automated sphygmomanometer (ES-H55, Terumo Co., Japan), which uses oscillometric methods.
Measurements of blood pressure were conducted in midmorning. Children were not requested
to be fasting. We used the appropriate size of blood pressure cuff based on each child's
arm circumference. As a rule, measurements were taken from the upper arm. The subjects
were measured in a sitting position after a few minutes of rest. The height and weight
of children were based on parents' reports. Body mass index (BMI) was calculated as
(weight in kg)/(height in m)2. From our subjects, we additionally obtained the measurements of the heights and
weights of 103 of the children. Among them, intra-class correlation coefficients between
measured and parent-reported data were 0.90, 0.96, and 0.78 in height, weight, and
BMI, respectively.

Statistical analysis

All analyses were performed separately for each sex. According to the nutrient density
method, we divided seaweed and salt intake by total energy intake, and presented them
as grams per 1,000 kcal of total energy. The dietary intakes such as total energy,
seaweed and salt were skewed and hence were logarithmic transformed in all analyses.

The characteristics by sex were calculated as mean (standard deviation: SD). The geometric
mean and 95% confidence interval were computed on the log-transformed values and converted
back to the original scale of measurement. We used Spearman's correlation coefficients
to detect the association of blood pressure and pulse with age, height, weight, BMI,
and intakes of total energy, salt or seaweed.

We divided the subjects into three groups according to tertile category (low, middle
or high) of seaweed intake. Tertiles were derived based on the distribution of seaweed
consumption in the current population. In order to elucidate the relationships of
seaweed intake with SBP, DBP and pulse, we used a one-way analysis of covariance (ANCOVA)
after adjustments for age and BMI. Tests for linear trend were performed on multiple
regression analyses using continues variables in seaweed intake.

All analyses were conducted using the SAS computer program, version 9.1 (SAS Institute).
All P values were calculated by a two-sided test. A P value of less than 0.05 was
considered statistically significant in all analyses.

Results

The characteristics of studied subjects are shown in Table 1. Subjects were 223 boys and 194 girls. The averages (SD) of SBP and DBP were, respectively,
98.7 (13.0) and 60.6 (11.1) mmHg among boys. Those were 99.5 (12.4) mmHg for SBP and
62.2 (11.8) mmHg for DBP among girls. The average pulse rate of girls was higher than
that of boys (93.6/min in boys and 96.5/min in girls: P = 0.047). Total energy intake was greater in boys than in girls (1446 kcal/day in
boys and 1337 kcal/day in girls: P < 0.001). The geometric means of seaweed intake were 0.67 and 0.76 g/day in boys and
girls, respectively (P = 0.096).

Table 3 shows the estimated means of SBP, DBP and pulse according to the tertile category
of dietary seaweed intake after adjustments for age and BMI. Boys with low, middle
and high intake of seaweed had DBP readings of 62.8, 59.3 and 59.6 mmHg, respectively
(P = 0.11, trend P = 0.038). Neither SBP nor pulse was associated with seaweed intake. Girls with higher
seaweed intake had significantly lower SBP than those with lower seaweed intake (P = 0.037, trend P = 0.030). The DBP of girls with low seaweed intake was higher than those of middle
and high intake of seaweed.

Table 3. Adjusted means of blood pressure and pulse according to the tertiles of dietary seaweed
intakea

Among seaweeds, nori (dried purple laver) was taken most common among our subjects
(geometrical mean: 0.37 g/day). The association of nori intake with blood pressure
was similar to that of total seaweed intake. For example, boys with low, middle and
high intake of nori had DBP readings of 61.4, 61.7 and 58.6 mmHg, respectively (trend
P = 0.057). Girls with low, middle and high intake of nori had SBP readings of 100.6,
101.1 and 97.0 mmHg, respectively (trend P = 0.040).

In order to see whether using parent-reported height and weight could influence the
results, we assessed the association between seaweed intake and blood pressure among
53 boys and 50 girls whose measurements of height and weight were obtained. When the
measured BMI was used as a confounder, boys with low, middle and high intake of seaweed
had DBP readings of 64.7, 57.7 and 54.8 mmHg, respectively (trend P = 0.075). Girls with low, middle and high intake of seaweed had SBP readings of 99.6,
98.9 and 92.5 mmHg, respectively (trend P = 0.032).

We repeated the same analyses including other dietary factors as a confounder. Salt
or sodium intake did not affect the negative association between seaweed intake and
DBP among boys. The negative association between seaweed intake and SBP was also unaltered
among girls. Additional adjustment for other mineral intakes (potassium, calcium,
magnesium) also did not change the associations observed. When vegetable, fruit or
fat intake was added as a confounder, the results were not substantially altered.

In addition, we assessed the association between seaweed intake and blood pressure
after additional adjustment for non-dietary lifestyle factors. Sleeping habits (sleeping
time in hours or the time when they got up or went to bed) or sedentary lifestyle
time (total minutes of watching television or video-gaming, and reading a book) did
not affect the association observed. We got data about physical activity only among
110 boys (Mean (SD): 98.0 (13.3) mmHg for SBP and 60.4 (12.1) mmHg for DBP) and 85
girls (Mean (SD): 98.5 (13.6) mmHg for SBP and 60.7 (SD: 10.2) mmHg for DBP). Although
the observed association became non- significant after additional adjustment for physical
activity, the tendency in the negative association between seaweed intake and blood
pressure was not altered. After additional adjustments for passive smoking or years
of mother's education, the negative association between seaweed intake and blood pressure
were observed.

Finally, we re-examined the association between seaweed intake and blood pressure
after excluding 4 children who took medications for common cold on the day of blood
pressure measurement. Along with the results among all subjects, seaweed intake was
negatively related to DBP in boys (trend P = 0.024) and to SBP in girls (trend P = 0.028).

Discussion

Although there is much evidence for dietary risk factors for hypertension in adults,
few studies of children have been reported [14-21]. Even the association between salt intake and blood pressure has been inconsistent
among children [14,15]. Several studies have demonstrated the negative associations of blood pressure with
calcium and magnesium among children [16-19], but very few researchers have examined whether the other dietary factors might affect
blood pressure in childhood [19-21]. To our knowledge, this study is the first to demonstrate an association between
seaweed intake and blood pressure in healthy children. Seaweed intake was negatively
related to DBP in boys and to SBP in girls. Although we cannot prove a causal relationship
because of a cross-sectional design of this study, the finding suggests that seaweed
might have beneficial effects on blood pressure among children.

Our study of 3- to 6-year-old Japanese children showed that the difference between
the highest and lowest tertiles was 3.5 mmHg in DBP among boys and 5.5 mmHg in SBP
among girls. Decreasing blood pressure in healthy children would be potentially beneficial
for blood pressure control in the future. Among Japanese adults aged 40 to 49 years,
the multivariate-adjusted hazard ratio of all-cause mortality for each 10-mmHg SBP
increase was reported to be 1.37 times in men and 1.19 in women during 9.8 years of
follow-up [34]. That for each 10-mm Hg DBP was 1.46 times in men and 1.40 times in women.

The negative association between seaweed and blood pressure in our study is supported
by the results of several experimental studies [23-27]. A diet containing powdered brown seaweed lowered blood pressure and reduced the
incidence of stroke in salt-loaded, stroke-prone spontaneously hypertensive rats [SHRs]
[23]. Hydrolysates of wakame (Undaria pinnatifida), a kind of seaweed, were reported to
decrease systolic blood pressure after oral administration in SHRs [24]. Peptides isolated from wakame also had inhibitory activity for angiotensin 1-conversing
enzyme, causing an antihypertensive effect [25-27]. In addition, Ikeda et al. found that the administration of wakame delayed the development
of stroke signs and improved the survival rate of salt-loaded, stroke-prone SHRs,
although there was no significant difference in blood pressure changes compared with
the control group [35]. These findings suggest that seaweed may have preventive effects on hypertension
and cerebrovascular diseases.

However, only a few epidemiological studies have reported an association between seaweed
intake and blood pressure, and the results have been inconsistent [28-31]. Among 62 middle-aged patients with mild hypertension in Sweden, Krotkiewski et al.
observed a significant decrease in mean blood pressure after the patients were given
12 and 24 g/day seaweed fiber for 4 weeks [28]. In hypertensive elderly Japanese patients, systolic and diastolic blood pressure
decreased after the patients received daily doses of 5 g of dried seaweed powder for
8 weeks [29]. In a cross-sectional study of 190 hypertensive elderly Japanese patients, the patients
treated with a low dose of a single drug ate more fruits and seaweed than the patients
treated with a high dose of a single drug or multiple drugs, which suggested that
the habitual intake of these food might help the control of blood pressure [30]. However, among 7,081 Korean men 30 years of age and older, participants with metabolic
syndrome, including hypertension, showed a higher intake of seaweed and oily foods
than did participants without metabolic syndrome [31]. These studies were conducted among adults, and, in this study, the relationship
of seaweed intake to blood pressure has been first demonstrated among children.

In our study, seaweed seemed to have greater relationships with DBP than SBP among
boys. Meanwhile, it seemed to have greater relationships with SBP than DBP among girls.
Although the effects of seaweed intake on blood pressure might be different in mechanism
between boys and girls, the reason for the discrepancy is unclear. In the studies
among adults, one study [31] included only men and the others [28-30] analyzed the association in mixed group of men and women. More reports are needed
to determine the association by sex.

The underlying mechanism responsible for the association between seaweed and blood
pressure remains to be clarified. Seaweed contains large quantities of minerals and
alginate, which is a kind of dietary fiber. Alginate has been reported to reduce blood
pressure [36], and Yamori et al. presumed that alginic acid in seaweed may cause the inhibition
of intentional sodium absorption [23]. Potassium, calcium and magnesium also have been reported to reduce blood pressure
in observational studies [13,16,17] and intervention trials [9-11,18]. However, the results among our subjects did not show associations between dietary
potassium, calcium and magnesium intake and blood pressure. Nonetheless, we cannot
deny the possibility that simultaneous intake of several minerals through seaweed
may be effective for blood pressure. Alternatively, other ingredients may play a role
in the control of blood pressure since alginate or each mineral in seaweed is lower
than the effective dose needed to lower blood pressure. The whole diet pattern including
seaweed intake is also possible to be responsible for the lower blood pressure.

Although a dietary record would be more accurate or better if it had been used for
a longer time or repeated over different seasons, using a dietary record was one of
merits in this study. One limitation is that blood pressure was measured only once,
which may have caused a large measurement error. However, it is unlikely that such
a measurement error was directly dependent on seaweed intake. Nonetheless, repeated
measurements are best practice and necessary in future studies. Another limitation
was that height and weight were reported by the parents. However, the correlation
coefficient between parents' reports and measured ones ranged from 0.90 to 0.96 for
height and 0.95 to 0.99 for weight among 170 first-grade and 206 fourth-grade Japanese
children [37]. In our supplementary analysis among 103 children, the intra-class correlation between
parent-reported and measured height and weight was high. Furthermore, the negative
associations between seaweed intake and blood pressure were observed among them after
the measured BMI was used as a confounder. Therefore, these differences would not
greatly change the associations observed in our study. We also must note that BMI
might not be necessarily a very good maker of fatness in growing children. Finally,
the generalizability of our study is limited by the fact that our subjects were ethnically
homogeneous Japanese children, whose diets differ from those of Western children.

Conclusions

We have demonstrated a negative association between dietary seaweed intake and blood
pressure among healthy children. Seaweed is a popular traditional foodstuff that is
widely eaten among both children and adults in Japan. Not only do our results suggest
that seaweed intake may have beneficial effects on blood pressure in children, but
they also provide the possibility of creating a new, earlier-in-life strategy for
the prevention of hypertension in adults.

Abbreviations

Authors' contributions

Author KW wrote the paper. Author CN designed the study and directed its implementation,
including quality assurance and control. Author KN helped designing the study's analytic
strategy. Author YT, MT, and YS conduct the literature review and prepare the Discussion
sections of the text. Author KW, SO, KY and KA helped supervise the field activities.
All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Acknowledgements

This work was supported by grants from the Ministry of Education, Culture, Sports,
Science and Technology, and the Ministry of Health, Labor and Welfare, and by Gifu
University Research Grant Program. None of the authors have financial interests related
to this paper.